Locomotion modulates olfactory learning through proprioception in C. elegans

Xu Zhan, Chao Chen, Longgang Niu, Xinran Du, Ying Lei, Rui Dan, Zhao-Wen Wang () and Ping Liu ()
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Xu Zhan: Tongji Medical College, Huazhong University of Science and Technology
Chao Chen: Huazhong University of Science and Technology
Longgang Niu: University of Connecticut School of Medicine
Xinran Du: University of Connecticut School of Medicine
Ying Lei: Tongji Medical College, Huazhong University of Science and Technology
Rui Dan: Tongji Medical College, Huazhong University of Science and Technology
Zhao-Wen Wang: University of Connecticut School of Medicine
Ping Liu: Tongji Medical College, Huazhong University of Science and Technology

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract Locomotor activities can enhance learning, but the underlying circuit and synaptic mechanisms are largely unknown. Here we show that locomotion facilitates aversive olfactory learning in C. elegans by activating mechanoreceptors in motor neurons, and transmitting the proprioceptive information thus generated to locomotion interneurons through antidromic-rectifying gap junctions. The proprioceptive information serves to regulate experience-dependent activities and functional coupling of interneurons that process olfactory sensory information to produce the learning behavior. Genetic destruction of either the mechanoreceptors in motor neurons, the rectifying gap junctions between the motor neurons and locomotion interneurons, or specific inhibitory synapses among the interneurons impairs the aversive olfactory learning. We have thus uncovered an unexpected role of proprioception in a specific learning behavior as well as the circuit, synaptic, and gene bases for this function.

Date: 2023
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DOI: 10.1038/s41467-023-40286-x

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